Improved isolation strategies allowed the phenotypic differentiation of two Nitrospira strains from widespread phylogenetic lineages

FEMS Microbiology Ecology

Volumn 91, Issue 3, 2015, Pages

  Nowka, Boris ^a   Off, Sandra ^a,c   Daims, Holger ^b   Spieck, Eva ^a  

^a UNIVERSITY OF HAMBURG   (Germany)

^b UNIVERSITY OF VIENNA   (Austria)

^c HAMBURG UNIVERSITY OF APPLIED SCIENCES   (Germany)

Author keywords

Diversity; Isolation; Nitrification; Nitrite oxidizing bacteria; Nitrospira; Physiology; Wastewater

Indexed keywords

ACTIVATED SLUDGE; ANTIBIOTIC RESISTANCE; ANTIBIOTICS; BACTERIUM; BIOFILM; ISOLATED POPULATION; LABORATORY METHOD; MOLECULAR ANALYSIS; NICHE; NITRATE; NITRIFICATION; NITRITE; OXIDATION; PHENOTYPE; PHYLOGENETICS; PHYSIOLOGY; SPECIES DIVERSITY; TOLERANCE; WASTEWATER;

BACTERIA (MICROORGANISMS); CANDIDATUS NITROSPIRA DEFLUVII; NITROSPIRA;

ACRIFLAVINE; AMPICILLIN; ANTIINFECTIVE AGENT; NITRIC ACID DERIVATIVE; NITRITE; RNA 16S; SEWAGE;

BACTERIUM; BIOFILM; CLASSIFICATION; ECOSYSTEM; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MULTIDRUG RESISTANCE; NITRIFICATION; OPTICAL TWEEZERS; OXIDATION REDUCTION REACTION; PHYLOGENY; SEWAGE;

ACRIFLAVINE; AMPICILLIN; ANTI-BACTERIAL AGENTS; BACTERIA; BIOFILMS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ECOSYSTEM; NITRATES; NITRIFICATION; NITRITES; OPTICAL TWEEZERS; OXIDATION-REDUCTION; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEWAGE;

EID: 84941231850     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1093/femsec/fiu031     Document Type: Article

References (68)

1. Alawi M, Lipski A, Sanders T, et al. Cultivation of a novel cold-adapted nitrite oxidizing betaproteobacterium fromthe Siberian Arctic. ISME J 2007;1:256-64.
2. Alawi M, OffS, Kaya M, et al. Temperature influences the population structure of nitrite-oxidizing bacteria in activated sludge. Environ Microbiol Rep 2009;1:184-90.
3. Altmann D, Stief P, Amann R, et al. In situ distribution and activity of nitrifying bacteria in freshwater sediment. Environ Microbiol 2003;5:798-803.
4. Altschul SF, Gish W, Miller W, et al. Basic local alignment search tool. J Mol Biol 1990;215:403-10.
5. Amann RI, Ludwig W, Schleifer KH. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 1995;59:143-69.
6. Bartosch S, Wolgast I, Spieck E, et al. Identification of nitriteoxidizing bacteria with monoclonal antibodies recognizing the nitrite oxidoreductase. Appl Environ Microb 1999;65:4126-33.
7. Boon B, Laudelout H. Kinetics of nitrite oxidation by Nitrobacter winogradskyi. Biochem J 1962;85:440-7.
8. Burrell PC, Keller J, Blackall LL. Microbiology of a nitrite-oxidizing bioreactor. Appl Environ Microb 1998;64:1878-83.
9. Chen Y, Wu L, Boden R, et al. Life without light: microbial diversity and evidence of sulfur- and ammonium-based chemolithotrophy in Movile Cave. ISME J 2009;3:1093-104.
10. Daims H. The family Nitrospiraceae. In: Rosenberg E, DeLong EF, Lory S, et al. (eds). The Prokaryotes, New York: Springer, 2014, 733-49.
11. Daims H, Nielsen JL, Nielsen PH, et al. In situ characterization of Nitrospira-like nitrite-oxidizing bacteria active in wastewater treatment plants. Appl Environ Microb 2001;67:5273-84.
12. Daims H, Wagner M. The microbiology of nitrogen removal. In:Seviour RJ, Nielsen PH (eds). The Microbiology of Activated Sludge. London, UK: IWA Publishing, 2010, 259.
13. Dolinsek J, Dorninger C, Lagkouvardos I, et al. Depletion of unwanted nucleic acid templates by selective cleavage:LNAzymes, catalytically active oligonucleotides containing locked nucleic acids, open a new window for detecting rare microbial community members. Appl Environ Microb 2013;79:1534-44.
14. Ehrich S, Behrens D, Lebedeva E, et al. A new obligately chemolithoautotrophic, nitrite-oxidizing bacterium, Nitrospira moscoviensis sp. nov. and its phylogenetic relationship. Arch Microbiol 1995;164:16-23.
15. Flemming HC, Wingender J. The biofilm matrix. Nat Rev Microbiol 2010;8:623-33.
16. Freitag TE, Chang L, Clegg CD, et al. Influence of inorganic nitrogen management regime on the diversity of nitrite-oxidizing bacteria in agricultural grassland soils. Appl Environ Microb 2005;71:8323-34.
17. Fujitani H, Ushiki N, Tsuneda S, et al. Isolation of sublineage I Nitrospira by a novel cultivation strategy. Environ Microbiol 2014;16:3030-40.
18. Gruber N, Galloway JN. An Earth-system perspective of the global nitrogen cycle. Nature 2008;451:293-6.
19. Gruber-Dorninger C, Pester M, Kitzinger K, et al. Functionally relevant diversity of closely related Nitrospira in activated sludge. ISME J 2014, DOI: 10.1038/ismej.2014.156.
20. He Q, He Z, Joyner DC, et al. Impact of elevated nitrate on sulfatereducing bacteria: a comparative study of Desulfovibrio vulgaris. ISME J 2010;4:1386-97.
21. Herpel N. The scale-dependent variability of topsoil properties reflecting ecosystem patchiness in drylands of Southern Africa. Dissertation. University of Hamburg 2008.
22. Hovanec TA, Taylor LT, Blakis A, et al. Nitrospira-like bacteria associated with nitrite oxidation in freshwater aquaria. Appl Environ Microb 1998;64:258-64.
23. Huber R, Burggraf S, Mayer T, et al. Isolation of a hyperthermophilic archaeum predicted by in situ RNA analysis. Nature 1995;376:57-8.
24. Johnson DB. Selective solid media for isolating and enumerating acidophilic bacteria. J Microbiol Meth 1995;23:205-18.
25. Juretschko S, Loy A, Lehner A, et al. The microbial community composition of a nitrifying-denitrifying activated sludge from an industrial sewage treatment plant analyzed by the full-cycle rRNA approach. Syst Appl Microbiol 2002;25:84-99.
26. Juretschko S, Timmermann G, Schmid M, et al. Combined molecular and conventional analyses of nitrifying bacterium diversity in activated sludge: Nitrosococcus mobilis and Nitrospiralike bacteria as dominant populations. Appl Environ Microb 1998;64:3042-51.
27. Keuter S, Kruse M, Lipski A, et al. Relevance of Nitrospira for nitrite oxidation in a marine recirculation aquaculture system and physiological features of a Nitrospira marina-like isolate. Environ Microbiol 2011;13:2536-47.
28. Kindaichi T, Ito T, Okabe S. Ecophysiological interaction between nitrifying bacteria and heterotrophic bacteria in autotrophic nitrifying biofilms as determined by microautoradiographyfluorescence in situ hybridization. Appl Environ Microb 2004;70:1641-50.
29. Kruse M, Zumbrägel S, Bakker E, et al. The nitrite-oxidizing community in activated sludge from a municipal wastewater treatment plant determined by fatty acid methyl ester-stable isotope probing. Syst Appl Microbiol 2013;36:517-24.
30. Kulp A, Kuehn MJ. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol 2010;64:163-84.
31. Lane DJ. 16S/23S rRNA sequencing. In:Stackebrandt E, Goodfellow M (eds). Nucleic Acid Techniques in Bacterial Systematics. Chichester, UK: John Wiley & Sons, 1991, 115.
32. Lebedeva EV, Alawi M, Fiencke C, et al. Moderately thermophilic nitrifying bacteria from a hot spring of the Baikal rift zone. FEMS Microbiol Ecol 2005;54:297-306.
33. Lebedeva EV, Alawi M, Maixner F, et al. Physiological and phylogenetic characterization of a novel lithoautotrophic nitriteoxidizing bacterium, 'Candidatus Nitrospira bockiana'. Int J Syst Evol Micr 2008;58:242-50.
34. Lebedeva EV, OffS, Zumbrägel S, et al. Isolation and characterization of a moderately thermophilic nitrite-oxidizing bacterium from a geothermal spring. FEMS Microbiol Ecol 2011;75:195-204.
35. Lerman LS. Acridine mutagens and DNA structure. J Cell Physiol 1964;64:1-18.
36. Lopez-Vazquez CM, Kubare M, Saroj DP, et al. Thermophilic biological nitrogen removal in industrial wastewater treatment. Appl Microbiol Biot 2014;98:945-56.
37. Lücker S, Wagner M, Maixner F, et al. A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria. P Natl Acad Sci USA 2010;107:13479-84.
38. Maixner F, Noguera DR, Anneser B, et al. Nitrite concentration influences the population structure of Nitrospira-like bacteria. Environ Microbiol 2006;8:1487-95.
39. Manz W, Amann R, Ludwig W, et al. Phylogenetic oligodeoxynucleotide probes for the major subclasses of proteobacteria:problems and solutions. Syst Appl Microbiol 1992;15:593-600.
40. Mashburn LM, Whiteley M. Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 2005;437:422-5.
41. Meincke M, Bock E, Kastrau D, et al. Nitrite oxidoreductase from Nitrobacter hamburgensis: redox centers and their catalytic role. Arch Microbiol 1992;158:127-31.
42. Muyzer G, deWaal EC, Uitterlinden AG. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microb 1993;59:695-700.
43. Nowka B, Daims H, Spieck E. Comparison of oxidation kinetics of nitrite-oxidizing bacteria: nitrite availability as a key factor in niche differentiation. Appl Environ Microb 2015 in press, DOI:10.1128/AEM.02734-14.
44. OffS. Nitrospira Schlüsselorganismus der Nitritoxidation in gemäßigten und extremen Lebensräumen. Dissertation. University of Hamburg, 2012.
45. OffS, Alawi M, Spieck E. Enrichment and physiological characterization of a novel Nitrospira-like bacterium obtained from a marine sponge. Appl Environ Microb 2010;76:4640-6.
46. Park HD, Noguera DR. Nitrospira community composition in nitrifying reactors operated with two different dissolved oxygen levels. J Microbiol Biotech 2008;18:1470-4.
47. Pester M, Maixner F, Berry D, et al. NxrB encoding the beta subunit of nitrite oxidoreductase as functional and phylogenetic marker for nitrite-oxidizing Nitrospira. Environ Microbiol 2014;16:3055-71.
48. Poly F, Wertz S, Brothier E, et al. First exploration of Nitrobacter diversity in soils by a PCR cloning-sequencing approach targeting functional gene nxrA. FEMS Microbiol Ecol 2007;63:132-40.
49. Remis JP, Costerton JW, Auer M. Biofilms: structures that may facilitate cell-cell interactions. ISME J 2010;4:1085-7.
50. Rittmann BE, Regan JM, Stahl DA. Nitrification as a source of soluble organic substrate in biological treatment. Water Sci Technol 1994;30:1-8.
51. Sanders T, Fiencke C, Spieck E, et al. Detection and enrichment of ammonia oxidizers from permafrost soils of Siberia. In: Kane DL, Hinkel KM (eds). Ninth International Conference on Permafrost, Vol. 2. Institute of Northern Engineering, University of Alaska Fairbanks 2008 printed in USA, 1567-71.
52. Sarbu SM, Kane TC, Kinkle BK. A chemoautotrophically based cave ecosystem. Science 1996;272:1953-5.
53. Schön G. Untersuchungen über den Nutzeffekt von Nitrobacter winogradskyi. Arch Microbiol 1965;50:111-32.
54. Schramm A, de Beer D, van den Heuvel JC, et al. Microscale distribution of populations and activities of Nitrosospira and Nitrospira spp. along a macroscale gradient in a nitrifying bioreactor:quantification by in situ hybridization and the use of microsensors. Appl Environ Microb 1999;65:3690-6.
55. Schramm A, de Beer D, Wagner M, et al. Identification and activities in situ of Nitrosospira and Nitrospira spp. as dominant populations in a nitrifying fluidized bed reactor. Appl Environ Microb 1998;64:3480-5.
56. Siripong S, Rittmann BE. Diversity study of nitrifying bacteria in full-scale municipal wastewater treatment plants. Water Res 2007;41:1110-20.
57. Smith PK, Krohn RI, Hermanson GT, et al. Measurement of protein using bicinchoninic acid. Anal Biochem 1985;150:76-85.
58. Sorokin DY, Lucker S, Vejmelkova D, et al. Nitrification expanded:discovery, physiology and genomics of a nitrite-oxidizing bacterium from the phylum Chloroflexi. ISME J 2012;6:2245-56.
59. Sorokin DY, Muyzer G, BrinkhoffT, et al. Isolation and characterization of a novel facultatively alkaliphilic Nitrobacter species, N. alkalicus sp. nov. Arch Microbiol 1998;170:345-52.
60. Spieck E, Hartwig C, McCormack I, et al. Selective enrichment and molecular characterization of a previously uncultured Nitrospira-like bacterium from activated sludge. Environ Microbiol 2006;8:405-15.
61. Spieck E, Keuter S, Wenzel T, et al. Characterization of a new marine nitrite oxidizing bacterium, Nitrospina watsonii sp. nov., a member of the newly proposed phylum 'Nitrospinae'. Syst Appl Microbiol 2014;37:170-6.
62. Spieck E, Lipski A. Cultivation, growth physiology, and chemotaxonomy of nitrite-oxidizing bacteria. Method Enzymol 2011;486:109-30.
63. Stackebrandt E, Ebers J. Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 2006;33:152-5.
64. Tamura K, Peterson D, Peterson N, et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011;28:2731-9.
65. Teske A, Alm E, Regan JM, et al. Evolutionary relationships among ammonia- and nitrite-oxidizing bacteria. J Bacteriol 1994;176:6623-30.
66. Ushiki N, Fujitani H, Aoi Y, et al. Isolation of Nitrospira belonging to sublineage II from a wastewater treatment plant. Microbes Environ 2013;28:346-53.
67. Watson SW, Bock E, Valois FW, et al. Nitrospira marina gen. nov. sp. nov.: a chemolithotrophic nitrite-oxidizing bacterium. Arch Microbiol 1986;144:1-7.
68. Zhang H, Fu H, Wang J, et al. Impacts of nitrate and nitrite on physiology of Shewanella oneidensis. PLoS one 2013;8:e62629.